pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence.
Identifieur interne : 001417 ( Main/Exploration ); précédent : 001416; suivant : 001418pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence.
Auteurs : Eva C. Boritsch [France] ; Wafa Frigui [France] ; Alessandro Cascioferro [France] ; Wladimir Malaga [France] ; Gilles Etienne [France] ; Françoise Laval [France] ; Alexandre Pawlik [France] ; Fabien Le Chevalier [France] ; Mickael Orgeur [France] ; Laurence Ma [France] ; Christiane Bouchier [France] ; Timothy P. Stinear [Australie] ; Philip Supply [France] ; Laleh Majlessi [France] ; Mamadou Daffé [France] ; Christophe Guilhot [France] ; Roland Brosch [France]Source :
- Nature microbiology [ 2058-5276 ] ; 2016.
Abstract
Mycobacterium tuberculosis is a major, globally spread, aerosol-transmitted human pathogen, thought to have evolved by clonal expansion from a Mycobacterium canettii-like progenitor. In contrast, extant M. canettii strains are rare, genetically diverse, and geographically restricted mycobacteria of only marginal epidemiological importance. Here, we show that the contrasting evolutionary success of these two groups is linked to loss of lipooligosaccharide biosynthesis and subsequent morphotype changes. Spontaneous smooth-to-rough M. canettii variants were found to be mutated in the polyketide-synthase-encoding pks5 locus and deficient in lipooligosaccharide synthesis, a phenotype restored by complementation. Importantly, these rough variants showed an altered host-pathogen interaction and increased virulence in cellular- and animal-infection models. In one variant, lipooligosaccharide deficiency occurred via homologous recombination between two pks5 genes and removal of the intervening acyltransferase-encoding gene. The resulting single pks5 configuration is similar to that fixed in M. tuberculosis, which is known to lack lipooligosaccharides. Our results suggest that pks5-recombination-mediated bacterial surface remodelling increased virulence, driving evolution from putative generalist mycobacteria towards professional pathogens of mammalian hosts.
DOI: 10.1038/nmicrobiol.2015.19
PubMed: 27571976
Affiliations:
- Australie, France
- Midi-Pyrénées, Occitanie (région administrative), Victoria (État), Île-de-France
- Melbourne, Paris, Toulouse
- Université de Melbourne
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tuberculosis emergence.</title><author><name sortKey="Boritsch, Eva C" sort="Boritsch, Eva C" uniqKey="Boritsch E" first="Eva C" last="Boritsch">Eva C. Boritsch</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Frigui, Wafa" sort="Frigui, Wafa" uniqKey="Frigui W" first="Wafa" last="Frigui">Wafa Frigui</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Cascioferro, Alessandro" sort="Cascioferro, Alessandro" uniqKey="Cascioferro A" first="Alessandro" last="Cascioferro">Alessandro Cascioferro</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Malaga, Wladimir" sort="Malaga, Wladimir" uniqKey="Malaga W" first="Wladimir" last="Malaga">Wladimir Malaga</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region></placeName></affiliation></author><author><name sortKey="Etienne, Gilles" sort="Etienne, Gilles" uniqKey="Etienne G" first="Gilles" last="Etienne">Gilles Etienne</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region></placeName></affiliation></author><author><name sortKey="Laval, Francoise" sort="Laval, Francoise" uniqKey="Laval F" first="Françoise" last="Laval">Françoise Laval</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region></placeName></affiliation></author><author><name sortKey="Pawlik, Alexandre" sort="Pawlik, Alexandre" uniqKey="Pawlik A" first="Alexandre" last="Pawlik">Alexandre Pawlik</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Le Chevalier, Fabien" sort="Le Chevalier, Fabien" uniqKey="Le Chevalier F" first="Fabien" last="Le Chevalier">Fabien Le Chevalier</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Orgeur, Mickael" sort="Orgeur, Mickael" uniqKey="Orgeur M" first="Mickael" last="Orgeur">Mickael Orgeur</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Ma, Laurence" sort="Ma, Laurence" uniqKey="Ma L" first="Laurence" last="Ma">Laurence Ma</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, PF1-Plate-Forme Génomique, Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, PF1-Plate-Forme Génomique, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name><affiliation wicri:level="3"><nlm:affiliation>Institut Pasteur, PF1-Plate-Forme Génomique, Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, PF1-Plate-Forme Génomique, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Stinear, Timothy P" sort="Stinear, Timothy P" uniqKey="Stinear T" first="Timothy P" last="Stinear">Timothy P. Stinear</name><affiliation wicri:level="4"><nlm:affiliation>Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria</wicri:regionArea><orgName type="university">Université de Melbourne</orgName><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Supply, Philip" sort="Supply, Philip" uniqKey="Supply P" first="Philip" last="Supply">Philip Supply</name><affiliation wicri:level="1"><nlm:affiliation>Inserm U1019, CNRS UMR8204, Université de Lille, Institut Pasteur de Lille, Center for Infection and Immunity, Lille 59000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Inserm U1019, CNRS UMR8204, Université de Lille, Institut Pasteur de Lille, Center for Infection and Immunity, Lille 59000</wicri:regionArea><wicri:noRegion>59000</wicri:noRegion><wicri:noRegion>59000</wicri:noRegion></affiliation></author><author><name sortKey="Majlessi, Laleh" sort="Majlessi, Laleh" uniqKey="Majlessi L" first="Laleh" last="Majlessi">Laleh Majlessi</name><affiliation wicri:level="1"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><wicri:noRegion>75015</wicri:noRegion><placeName><settlement type="city">Paris</settlement><region type="région" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Daffe, Mamadou" sort="Daffe, Mamadou" uniqKey="Daffe M" first="Mamadou" last="Daffé">Mamadou Daffé</name><affiliation wicri:level="1"><nlm:affiliation>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000</wicri:regionArea><wicri:noRegion>31000</wicri:noRegion><placeName><settlement type="city">Toulouse</settlement><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region></placeName></affiliation></author><author><name sortKey="Guilhot, Christophe" sort="Guilhot, Christophe" uniqKey="Guilhot C" first="Christophe" last="Guilhot">Christophe Guilhot</name><affiliation wicri:level="1"><nlm:affiliation>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IPBS (Institut de Pharmacologie et de Biologie Structurale), Toulouse 31000</wicri:regionArea><wicri:noRegion>31000</wicri:noRegion><placeName><settlement type="city">Toulouse</settlement><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region></placeName></affiliation></author><author><name sortKey="Brosch, Roland" sort="Brosch, Roland" uniqKey="Brosch R" first="Roland" last="Brosch">Roland Brosch</name><affiliation wicri:level="1"><nlm:affiliation>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris 75015</wicri:regionArea><wicri:noRegion>75015</wicri:noRegion><placeName><settlement type="city">Paris</settlement><region type="région" nuts="2">Île-de-France</region></placeName></affiliation></author></analytic><series><title level="j">Nature microbiology</title><idno type="eISSN">2058-5276</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Mycobacterium tuberculosis is a major, globally spread, aerosol-transmitted human pathogen, thought to have evolved by clonal expansion from a Mycobacterium canettii-like progenitor. In contrast, extant M. canettii strains are rare, genetically diverse, and geographically restricted mycobacteria of only marginal epidemiological importance. Here, we show that the contrasting evolutionary success of these two groups is linked to loss of lipooligosaccharide biosynthesis and subsequent morphotype changes. Spontaneous smooth-to-rough M. canettii variants were found to be mutated in the polyketide-synthase-encoding pks5 locus and deficient in lipooligosaccharide synthesis, a phenotype restored by complementation. Importantly, these rough variants showed an altered host-pathogen interaction and increased virulence in cellular- and animal-infection models. In one variant, lipooligosaccharide deficiency occurred via homologous recombination between two pks5 genes and removal of the intervening acyltransferase-encoding gene. The resulting single pks5 configuration is similar to that fixed in M. tuberculosis, which is known to lack lipooligosaccharides. Our results suggest that pks5-recombination-mediated bacterial surface remodelling increased virulence, driving evolution from putative generalist mycobacteria towards professional pathogens of mammalian hosts.</div></front></TEI><affiliations><list><country><li>Australie</li><li>France</li></country><region><li>Midi-Pyrénées</li><li>Occitanie (région administrative)</li><li>Victoria (État)</li><li>Île-de-France</li></region><settlement><li>Melbourne</li><li>Paris</li><li>Toulouse</li></settlement><orgName><li>Université de Melbourne</li></orgName></list><tree><country name="France"><region name="Île-de-France"><name sortKey="Boritsch, Eva C" sort="Boritsch, Eva C" uniqKey="Boritsch E" first="Eva C" last="Boritsch">Eva C. Boritsch</name></region><name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name><name sortKey="Brosch, Roland" sort="Brosch, Roland" uniqKey="Brosch R" first="Roland" last="Brosch">Roland Brosch</name><name sortKey="Cascioferro, Alessandro" sort="Cascioferro, Alessandro" uniqKey="Cascioferro A" first="Alessandro" last="Cascioferro">Alessandro Cascioferro</name><name sortKey="Daffe, Mamadou" sort="Daffe, Mamadou" uniqKey="Daffe M" first="Mamadou" last="Daffé">Mamadou Daffé</name><name sortKey="Etienne, Gilles" sort="Etienne, Gilles" uniqKey="Etienne G" first="Gilles" last="Etienne">Gilles Etienne</name><name sortKey="Frigui, Wafa" sort="Frigui, Wafa" uniqKey="Frigui W" first="Wafa" last="Frigui">Wafa Frigui</name><name sortKey="Guilhot, Christophe" sort="Guilhot, Christophe" uniqKey="Guilhot C" first="Christophe" last="Guilhot">Christophe Guilhot</name><name sortKey="Laval, Francoise" sort="Laval, Francoise" uniqKey="Laval F" first="Françoise" last="Laval">Françoise Laval</name><name sortKey="Le Chevalier, Fabien" sort="Le Chevalier, Fabien" uniqKey="Le Chevalier F" first="Fabien" last="Le Chevalier">Fabien Le Chevalier</name><name sortKey="Ma, Laurence" sort="Ma, Laurence" uniqKey="Ma L" first="Laurence" last="Ma">Laurence Ma</name><name sortKey="Majlessi, Laleh" sort="Majlessi, Laleh" uniqKey="Majlessi L" first="Laleh" last="Majlessi">Laleh Majlessi</name><name sortKey="Malaga, Wladimir" sort="Malaga, Wladimir" uniqKey="Malaga W" first="Wladimir" last="Malaga">Wladimir Malaga</name><name sortKey="Orgeur, Mickael" sort="Orgeur, Mickael" uniqKey="Orgeur M" first="Mickael" last="Orgeur">Mickael Orgeur</name><name sortKey="Pawlik, Alexandre" sort="Pawlik, Alexandre" uniqKey="Pawlik A" first="Alexandre" last="Pawlik">Alexandre Pawlik</name><name sortKey="Supply, Philip" sort="Supply, Philip" uniqKey="Supply P" first="Philip" last="Supply">Philip Supply</name></country><country name="Australie"><region name="Victoria (État)"><name sortKey="Stinear, Timothy P" sort="Stinear, Timothy P" uniqKey="Stinear T" first="Timothy P" last="Stinear">Timothy P. Stinear</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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